Unveiling tomato defense mechanisms against Bradysia impatiens (Diptera: Sciaridae) feeding: insights from transcriptomic and metabolomic analyses

Abstract

Tomato (Solanum lycopersicum) is an important agricultural crop frequently threatened by pests such as Bradysia impatiens (B. impatiens), a globally distributed sciarid fly whose larvae inflict severe damage on roots, stems, and leaves, leading to substantial yield losses. Despite its economic importance, the molecular and metabolic mechanisms underlying tomato defense against B. impatiens remain poorly understood. In this study, integrated transcriptomic and metabolomic approaches were employed to investigate the responses of tomato leaves to B. impatiens larval infestation at one week post-infestation. In our experimental system, larvae were introduced onto the soil surface and sequentially fed on stem bases (causing seedling lodging), leaves of prostrate plants, and roots. The leaf responses therefore reflect a combination of direct larval feeding on leaf tissues and systemic effects resulting from stem and root damage. Herbivory induced extensive transcriptional reprogramming, with 2,973 differentially expressed genes (DEGs) significantly enriched in pathways related to MAPK signaling, plant hormone transduction, plant-pathogen interactions, and phenylpropanoid biosynthesis. Metabolomic analysis identified 1,462 differentially accumulated metabolites, indicating significant shifts in energy metabolism, antioxidant defense systems, and the biosynthesis of defense-related compounds such as terpenoids and phenylpropanoids. Combined analyses revealed synchronized induction of α-linolenic acid metabolism and jasmonate signaling, accompanied by increased accumulation of reactive oxygen species (ROS) and upregulation of ethylene-responsive factors (ERF), bHLH, and NAC transcription factors. These findings reveal a tiered defensive regulatory network in tomato that integrates signal perception, hormonal regulation, metabolic reconfiguration, and ROS-mediated responses to counteract B. impatiens infestation. This entire defensive cascade embodies herbivory-triggered induced resistance, accompanied by sustained adaptive metabolic remodeling to withstand continuous larval feeding pressure. This study provides a comprehensive perspective on tomato plant-insect interactions and identifies potential targets for enhancing tomato resistance through molecular breeding or ecological management strategies. Notably, the hub transcription factor gene MYC, JA rate-limiting biosynthetic gene 12-oxophytodienoate reductase 3 (OPR3), α-linolenic acid-derived oxylipins and phenylpropanoid metabolites are highlighted as promising molecular biomarkers and core targets for future tomato anti-fungus gnat resistance engineering.